Shorter-duration escapes driven by Drosophila giant interneurons promote survival during predation

Large axon-diameter descending neurons are metabolically costly but transmit information rapidly from sensory neurons in the brain to motor neurons in the nerve cord. They have thus endured as a common feature of escape circuits in many animal species where speed is paramount. Though often considered isolated command neurons triggering fast-reaction-time, all-or-none escape responses, giant neurons are one of multiple parallel pathways enabling selection between behavioural alternatives. Such degeneracy among escape circuits makes it unclear if and how giant neurons benefit prey fitness. Here we competed Drosophila melanogaster flies with genetically silenced giant fibres (GFs) against flies with functional GFs in an arena with wild-caught damselfly predators and found that GF silencing decreases prey survival. Kinematic analysis of damselfly attack trajectories shows that decreased prey survival results from predator capture of GF-silenced flies during some attack speeds and approach distances that would normally elicit successful escapes. In previous studies with a virtual looming stimulus, we proposed a model in which GFs enforce the selection of a short-duration take-off sequence as opposed to reducing reaction time. Our findings here demonstrate that, during real predation scenarios, the GFs indeed promote prey survival by influencing action selection as a means to increase escape probability.